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The Root Hair “Infectome” Of Medicago Truncatula Uncovers Changes In Cell Cycle Genes And Reveals A Requirement For Auxin Signaling In Rhizobial Infection[W][OPEN]

A. Breakspear, Chengwu Liu, Sonali Roy, N. Stacey, C. Rogers, M. Trick, Giulia Morieri, K. Mysore, J. Wen, G. Oldroyd, J. Downie, J. Murray
Published 2014 · Biology, Medicine

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Transcriptome profiling of M. truncatula root hairs during the initial stages of rhizobial infection helps to interpret two decades of research on Medicago and provides a foundation for future studies on host-symbiont interactions in the rhizosphere. Nitrogen-fixing rhizobia colonize legume roots via plant-made intracellular infection threads. Genetics has identified some genes involved but has not provided sufficient detail to understand requirements for infection thread development. Therefore, we transcriptionally profiled Medicago truncatula root hairs prior to and during the initial stages of infection. This revealed changes in the responses to plant hormones, most notably auxin, strigolactone, gibberellic acid, and brassinosteroids. Several auxin responsive genes, including the ortholog of Arabidopsis thaliana Auxin Response Factor 16, were induced at infection sites and in nodule primordia, and mutation of ARF16a reduced rhizobial infection. Associated with the induction of auxin signaling genes, there was increased expression of cell cycle genes including an A-type cyclin and a subunit of the anaphase promoting complex. There was also induction of several chalcone O-methyltransferases involved in the synthesis of an inducer of Sinorhizobium meliloti nod genes, as well as a gene associated with Nod factor degradation, suggesting both positive and negative feedback loops that control Nod factor levels during rhizobial infection. We conclude that the onset of infection is associated with reactivation of the cell cycle as well as increased expression of genes required for hormone and flavonoid biosynthesis and that the regulation of auxin signaling is necessary for initiation of rhizobial infection threads.
This paper references
The infection process
P. J. Dart (1974)
Sur l’état diploide des cellules du méritème des nodules radiculaires des légumineuses
G. Truchet (1978)
10.1139/M80-092
Sensitivity of Rhizobium to selected isoflavonoids.
C. E. Pankhurst (1980)
10.1016/B978-0-12-509001-8.50011-1
Chapter 3 – The Infection Process
R. Goodman (1982)
10.1111/J.1399-3054.1986.TB05954.X
Rhizobium induces marked root hair curling by redirection of tip growth: a computer simulation
F. D. H. Batenburg (1986)
10.1038/323632A0
Flavones induce expression of nodulation genes in Rhizobium
J. Redmond (1986)
10.1126/SCIENCE.3738520
A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes.
N. Peters (1986)
10.1002/j.1460-2075.1987.tb02351.x
Clovers secrete specific phenolic compounds which either stimulate or repress nod gene expression in Rhizobium trifolii
M. Djordjevic (1987)
10.1016/S0176-1617(87)80166-9
Regulation of the Plane of Cell Division in Vacuolated Cells I. The Function of Nuclear Positioning and Phragmosome Formation
C. J. Venverloo (1987)
10.1111/J.1399-3054.1987.TB01955.X
Isolation of root hairs from seedlings of Pisum sativum. Identification of root hair specific proteins by in situ labeling
M. Röhm (1987)
10.1104/PP.88.2.396
Alfalfa Root Exudates and Compounds which Promote or Inhibit Induction of Rhizobium meliloti Nodulation Genes.
N. Peters (1988)
10.1104/PP.91.3.842
A Chalcone and Two Related Flavonoids Released from Alfalfa Roots Induce nod Genes of Rhizobium meliloti.
C. Maxwell (1989)
10.1128/jb.172.9.5394-5401.1990
A biovar-specific signal of Rhizobium leguminosarum bv. viciae induces increased nodulation gene-inducing activity in root exudate of Vicia sativa subsp. nigra
A. V. van Brussel (1990)
The Cytoskeletal basis of plant growth and form
C. Lloyd (1991)
10.1146/ANNUREV.CB.07.110191.001203
Development of the legume root nodule.
N. Brewin (1991)
10.1104/PP.97.1.7
Stress Responses in Alfalfa (Medicago sativa L.): X. Molecular Cloning and Expression of S-Adenosyl-l-Methionine:Caffeic Acid 3-O-Methyltransferase, a Key Enzyme of Lignin Biosynthesis.
G. Gowri (1991)
10.1128/JB.173.11.3432-3439.1991
Isoflavonoid-inducible resistance to the phytoalexin glyceollin in soybean rhizobia.
M. Parniske (1991)
Cytoskeletal elements of the phragmosome establish the division plane in vacuolated higher plant cells
C. W. Lloyd (1991)
10.1126/science.257.5066.70
Induction of Pre-Infection Thread Structures in the Leguminous Host Plant by Mitogenic Lipo-Oligosaccharides of Rhizobium
A. V. van Brussel (1992)
10.1111/j.1365-2958.1992.tb01535.x
Rhizobium leguminosarum has two glucosamine syntheses, GImS and NodM, required for nodulation and development of nitrogen‐fixing nodules
C. Marie (1992)
10.1016/0003-9861(92)90379-B
Identification, purification, and characterization of S-adenosyl-L-methionine: isoliquiritigenin 2'-O-methyltransferase from alfalfa (Medicago sativa L.).
C. A. Maxwell (1992)
Identification, purification, and characterization of S-adenosyl-L-methionine: isoliquiritigenin 29-O-methyltransferase from alfalfa (Medicago sativa L.)
C. A. Maxwell (1992)
10.1104/pp.101.3.819
Alfalfa (Medicago sativa L.) Root Exudates Contain Isoflavonoids in the Presence of Rhizobium meliloti
F. Dakora (1993)
10.1094/MPMI-7-0740
ENOD12 gene expression as a molecular marker for comparing Rhizobium-dependent and -independent nodulation in alfalfa
M. Pichon (1994)
10.1105/tpc.6.10.1415
Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation.
W. C. Yang (1994)
10.1007/978-94-011-0177-6_16
Effects of Nod Factors on Alfalfa Root Hair Ca ++ and H + Currents and on Cytoskeletal Behavior
N. S. Allen (1994)
Conversion of vestitone to medicarpin in alfalfa (Medicago sativa L.) is catalyzed by two independent enzymes. Identification, purification, and characterization of vestitone reductase and 7,2'-dihydroxy-4'-methoxyisoflavanol dehydratase.
L. Guo (1994)
10.1104/pp.106.1.37
An Auxin-Inducible Element in Soybean SAUR Promoters
Y. Li (1994)
10.1007/978-94-011-0177-6
Advances in Molecular Genetics of Plant-Microbe Interactions
M. Daniels (1994)
10.1016/0003-9861(95)90019-5
Molecular cloning and expression of alfalfa (Medicago sativa L.) vestitone reductase, the penultimate enzyme in medicarpin biosynthesis.
L. Guo (1995)
10.1105/TPC.7.11.1847
The D-type alfalfa cyclin gene cycMs4 complements G1 cyclin-deficient yeast and is induced in the G1 phase of the cell cycle.
M. Dahl (1995)
10.1105/tpc.7.10.1611
Composite structure of auxin response elements.
T. Ulmasov (1995)
10.1105/TPC.7.6.759
cycMs3, a novel B-type alfalfa cyclin gene, is induced in the G0-to-G1 transition of the cell cycle.
I. Meskiene (1995)
10.1105/tpc.7.1.43
Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti.
D. Cook (1995)
10.1104/pp.108.4.1607
Lipo-chitooligosaccharide Nodulation Signals from Rhizobium meliloti Induce Their Rapid Degradation by the Host Plant Alfalfa
C. Staehelin (1995)
10.1046/J.1365-313X.1996.10020295.X
Rapid alkalinization in alfalfa root hairs in response to rhizobial lipochitooligosaccharide signals
H. Felle (1996)
10.1126/SCIENCE.275.5299.527
A Legume Ethylene-Insensitive Mutant Hyperinfected by Its Rhizobial Symbiont
R. Penmetsa (1997)
10.1046/J.1365-313X.1997.11020277.X
Distinct response of Medicago suspension cultures and roots to Nod factors and chitin oligomers in the elicitation of defense‐related responses
A. Savouré (1997)
10.1105/tpc.9.11.1963
Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.
T. Ulmasov (1997)
10.1104/PP.117.4.1325
Expressed sequence tags from a root-hair-enriched medicago truncatula cDNA library
Covitz (1998)
10.1046/J.1365-313X.1998.00321.X
Auxin and ethylene promote root hair elongation in Arabidopsis.
R. Pitts (1998)
10.1046/J.1365-313X.1998.00245.X
Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling.
D. Laudert (1998)
10.1104/PP.116.3.871
Rearrangement of actin microfilaments in plant root hairs responding to rhizobium etli nodulation signals
Crdenas (1998)
10.1046/J.1365-313X.1998.00090.X
Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides.
U. Mathesius (1998)
10.1007/s004380050995
Genomic organization and expression properties of the MtSucS1 gene, which encodes a nodule-enhanced sucrose synthase in the model legume Medicago truncatula
N. Hohnjec (1999)
10.1038/46058
A plant regulator controlling development of symbiotic root nodules
L. Schauser (1999)
Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements.
A. Timmers (1999)
10.1094/MPMI.1999.12.9.829
Rhizobium Nod Factors Induce an Increase in Sub-apical Fine Bundles of Actin Filaments in Vicia sativa Root Hairs within Minutes
N. Ruijter (1999)
10.1093/emboj/18.16.4476
The mitotic inhibitor ccs52 is required for endoreduplication and ploidy‐dependent cell enlargement in plants
Á. Cebolla (1999)
The mitotic inhibitor
A. Cebolla (1999)
10.1094/MPMI.2000.13.4.413
Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum.
J. Wisniewski (2000)
10.1186/gb-2002-3-7-research0034
Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes
J. Vandesompele (2001)
10.1105/TPC.010289
AUX/IAA Proteins Are Active Repressors, and Their Stability and Activity Are Modulated by Auxin Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010289.
S. Tiwari (2001)
10.1105/TPC.010193
Ethylene Inhibits the Nod Factor Signal Transduction Pathway of Medicago truncatula
Giles E. D. Oldroyd (2001)
10.1094/MPMI.2001.14.6.695
Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations.
A. Boisson-Dernier (2001)
10.1094/MPMI.2001.14.6.737
Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells.
E. Journet (2001)
10.1046/J.1365-313X.2002.01429.X
The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula.
Fernanda de Carvalho-Niebel (2002)
10.1055/S-2002-37407
Mtha1, a Plasma Membrane H+-ATPase Gene from Medicago truncatula, Shows Arbuscule-Specific Induced Expression in Mycorrhizal Tissue
F. Krajinski (2002)
10.1094/MPMI.2002.15.6.522
Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula.
S. Ramu (2002)
10.1021/BI0255266
Role of hydrogen bonds in the reaction mechanism of chalcone isomerase.
J. Jez (2002)
The H + - ATPase HA 1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis
F. Krajinski (2002)
10.1104/pp.102.010710
Identification and Characterization of Nodulation-Signaling Pathway 2, a Gene of Medicago truncatula Involved in Nod Factor Signaling1
G. Oldroyd (2003)
10.1104/pp.103.021634
Nod Factor-Induced Root Hair Curling: Continuous Polar Growth towards the Point of Nod Factor Application1
J. Esseling (2003)
10.1104/pp.103.028662
Brassinosteroids Promote Root Growth in Arabidopsis
C. Müssig (2003)
10.1038/nature02039
Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases
S. Radutoiu (2003)
10.1105/tpc.008417
The Roles of Auxin Response Factor Domains in Auxin-Responsive Transcription Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008417.
S. Tiwari (2003)
Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod actor signaling.
G. Oldroyd (2003)
10.1080/10635150390235520
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.
S. Guindon (2003)
10.1093/JXB/ERG245
A method for the isolation of root hairs from the model legume Medicago truncatula.
J. Ramos (2003)
Nod factorinduced root hair curling: continuous polar growth towards the point of nod factor application
J. J. Esseling (2003)
10.1007/BF02183086
Synthesis, release, and transmission of alfalfa signals to rhizobial symbionts
D. Phillips (2004)
10.1016/S0092-8674(04)00300-9
Cyclin C/Cdk3 Promotes Rb-Dependent G0 Exit
S. Ren (2004)
10.1016/J.TPLANTS.2004.09.002
Performing the paradoxical: how plant peroxidases modify the cell wall.
F. Passardi (2004)
10.1007/s00425-004-1268-8
Sinorhizobium meliloti-induced chitinase gene expression in Medicago truncatula ecotype R108-1: a comparison between symbiosis-specific class V and defence-related class IV chitinases
P. Salzer (2004)
10.1093/NAR/GKH340
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
R. Edgar (2004)
10.1007/BF01322618
Regulation of the plane of cell division in vacuolated cells
C. J. Venverloo (2005)
10.1038/nature03608
Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi
K. Akiyama (2005)
10.1093/JXB/ERI244
Transcript enrichment of Nod factor-elicited early nodulin genes in purified root hair fractions of the model legume Medicago truncatula.
L. Sauviac (2005)
10.1104/pp.104.056572
Overlaps in the Transcriptional Profiles of Medicago truncatula Roots Inoculated with Two Different Glomus Fungi Provide Insights into the Genetic Program Activated during Arbuscular Mycorrhiza1[w]
N. Hohnjec (2005)
10.1016/J.PBI.2005.05.013
Nod factor signaling genes and their function in the early stages of Rhizobium infection.
R. Geurts (2005)
10.1105/tpc.105.033076
Control of Root Cap Formation by MicroRNA-Targeted Auxin Response Factors in Arabidopsisw⃞
Jia-Wei Wang (2005)
10.1093/JXB/ERI122
Ectopic endoreduplication caused by sterol alteration results in serrated petals in Arabidopsis.
Y. Hase (2005)
10.1126/SCIENCE.1111025
NSP1 of the GRAS Protein Family Is Essential for Rhizobial Nod Factor-Induced Transcription
P. Smit (2005)
10.1105/tpc.104.027987
DISTORTED3/SCAR2 Is a Putative Arabidopsis WAVE Complex Subunit That Activates the Arp2/3 Complex and Is Required for Epidermal Morphogenesis
Dipanwita Basu (2005)
10.1080/10635150590947131
Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary.
M. Lavin (2005)
10.1104/pp.105.062414
Nodulation Phenotypes of Gibberellin and Brassinosteroid Mutants of Pea1
B. Ferguson (2005)
10.1126/SCIENCE.1110951
Nodulation Signaling in Legumes Requires NSP2, a Member of the GRAS Family of Transcriptional Regulators
P. Kaló (2005)
10.1104/pp.106.089508
Lotus japonicus Nodulation Requires Two GRAS Domain Regulators, One of Which Is Functionally Conserved in a Non-Legume1[C][W]
A. Heckmann (2006)
10.1111/J.1365-313X.2006.02874.X
Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum.
S. Subramanian (2006)
10.1105/tpc.105.039156
The Arabidopsis-mei2-Like Genes Play a Role in Meiosis and Vegetative Growth in Arabidopsis[W]
J. Kaur (2006)
10.1080/10635150600755453
Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative.
M. Anisimova (2006)
10.1105/tpc.106.046417
The Cauliflower Or Gene Encodes a DnaJ Cysteine-Rich Domain-Containing Protein That Mediates High Levels of β-Carotene Accumulation[W]
Shan Lu (2006)
10.1038/nrm1988
The anaphase promoting complex/cyclosome: a machine designed to destroy
J. Peters (2006)
10.7490/f1000research.1056.1
Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia.
A. Wasson (2006)
10.1242/dev.02654
The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis
C. Spitzer (2006)
10.1101/GAD.402806
MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula.
J. Combier (2006)
10.1385/1-59745-130-4:301
Alfalfa (Medicago sativa L.).
D. Samac (2006)
10.1186/gb-2007-8-2-r19
qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data
J. Hellemans (2006)
10.1104/pp.106.080093
The Ethylene-Insensitive sickle Mutant of Medicago truncatula Shows Altered Auxin Transport Regulation during Nodulation1[W]
J. Prayitno (2006)
The Arabidopsis-mei2like genes play a role in meiosis and vegetative growth in Arabidopsis
J. Kaur (2006)
The Ethyleneinsensitive sickle mutant of Medicago truncatula shows altered auxin transport regulation during nodulation
J. Prayitno (2006)
10.1007/s00425-007-0558-3
Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis
C. Do (2007)
10.1104/pp.107.101337
Auxin Influx Activity Is Associated with Frankia Infection during Actinorhizal Nodule Formation in Casuarina glauca1[C][W][OA]
B. Péret (2007)
10.1105/tpc.107.053728
Nucleocytoplasmic Shuttling of BZR1 Mediated by Phosphorylation Is Essential in Arabidopsis Brassinosteroid Signaling[W][OA]
Hojin Ryu (2007)
10.1094/MPMI-20-2-0129
Nod factor perception during infection thread growth fine-tunes nodulation.
Jeroen Den Herder (2007)
10.1104/pp.107.103788
Phosphate Starvation Root Architecture and Anthocyanin Accumulation Responses Are Modulated by the Gibberellin-DELLA Signaling Pathway in Arabidopsis1[OA]
Caifu Jiang (2007)
10.1126/SCIENCE.1132514
A Cytokinin Perception Mutant Colonized by Rhizobium in the Absence of Nodule Organogenesis
J. Murray (2007)
10.1104/pp.106.093021
Medicago truncatula NIN Is Essential for Rhizobial-Independent Nodule Organogenesis Induced by Autoactive Calcium/Calmodulin-Dependent Protein Kinase1
J. F. Marsh (2007)
10.1105/tpc.106.048264
An ERF Transcription Factor in Medicago truncatula That Is Essential for Nod Factor Signal Transduction[W]
P. H. Middleton (2007)
10.1016/J.TPLANTS.2007.06.006
Distinct, crucial roles of flavonoids during legume nodulation.
S. Subramanian (2007)
10.1104/pp.106.095018
Flavone Synthases from Medicago truncatula Are Flavanone-2-Hydroxylases and Are Important for Nodulation1[W][OA]
J. Zhang (2007)
10.1104/pp.107.100495
Medicago LYK3, an Entry Receptor in Rhizobial Nodulation Factor Signaling1[W]
P. Smit (2007)
10.1073/pnas.0708586104
Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs
G. Monshausen (2007)
10.1104/pp.107.106955
Antisense Repression of the Medicago truncatula Nodule-Enhanced Sucrose Synthase Leads to a Handicapped Nitrogen Fixation Mirrored by Specific Alterations in the Symbiotic Transcriptome and Metabolome1[W]
M. Baier (2007)
10.1105/tpc.107.052944
AP2-ERF Transcription Factors Mediate Nod Factor–Dependent Mt ENOD11 Activation in Root Hairs via a Novel cis-Regulatory Motif[W]
Andry Andriankaja (2007)
10.1016/J.JMB.2007.03.040
Crystal structure of vestitone reductase from alfalfa (Medicago sativa L.).
H. Shao (2007)
10.1105/tpc.106.048041
ABA Is an Essential Signal for Plant Resistance to Pathogens Affecting JA Biosynthesis and the Activation of Defenses in Arabidopsis[W]
B. Adie (2007)
10.1104/pp.108.125674
Mechanism of Infection Thread Elongation in Root Hairs of Medicago truncatula and Dynamic Interplay with Associated Rhizobial Colonization1[W][OA]
J. Fournier (2008)
10.1186/1471-2229-9-10
Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis
S. K. Gomez (2008)
10.1111/J.1365-313X.2008.03509.X
Nucleocytoplasmic-localized acyltransferases catalyze the malonylation of 7-O-glycosidic (iso)flavones in Medicago truncatula.
Xiao-Hong Yu (2008)
10.1104/pp.108.131649
Establishment of a Protein Reference Map for Soybean Root Hair Cells1[W][OA]
L. Brechenmacher (2008)
10.1073/pnas.0710273105
The RPG gene of Medicago truncatula controls Rhizobium-directed polar growth during infection
J. Arrighi (2008)
10.1111/j.1365-313X.2008.03519.x
A gene expression atlas of the model legume Medicago truncatula.
V. Benedito (2008)
10.1111/j.0960-7412.2008.03509.x
Nucleocytoplasmic-localized acyltransferases catalyze the malonylation of 7-O-glycosidic (iso)flavones in Medicago truncatula.
Xiaohong Yu (2008)
10.1186/1471-2229-8-110
Genome-wide transcriptional analysis of super-embryogenic Medicago truncatula explant cultures
N. Imin (2008)
10.1101/gad.461808
Trans-regulation of the expression of the transcription factor MtHAP2-1 by a uORF controls root nodule development.
J. Combier (2008)
10.1111/j.1365-313X.2008.03427.x
Arabidopsis DMR6 encodes a putative 2OG-Fe(II) oxygenase that is defense-associated but required for susceptibility to downy mildew.
M. van Damme (2008)
10.1104/pp.109.143933
LIN, a Novel Type of U-Box/WD40 Protein, Controls Early Infection by Rhizobia in Legumes1[C][W][OA]
E. Kiss (2009)
10.1111/j.1365-313X.2008.03676.x
Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti.
J. Zhang (2009)
10.1104/pp.109.148379
Complete Transcriptome of the Soybean Root Hair Cell, a Single-Cell Model, and Its Alteration in Response to Bradyrhizobium japonicum Infection1[C][W][OA]
M. Libault (2009)
10.4161/psb.4.9.9395
Genetic analysis of ethylene regulation of legume nodulation
P. Gresshoff (2009)
10.1073/pnas.0910081107
Plant flotillins are required for infection by nitrogen-fixing bacteria
C. H. Haney (2009)
10.1105/tpc.108.063693
Rearrangement of Actin Cytoskeleton Mediates Invasion of Lotus japonicus Roots by Mesorhizobium loti[C][W]
Keisuke Yokota (2009)
10.1104/pp.109.149898
Knockdown of the Symbiotic Sucrose Synthase MtSucS1 Affects Arbuscule Maturation and Maintenance in Mycorrhizal Roots of Medicago truncatula1[W]
M. Baier (2009)
10.1111/j.1365-313X.2009.04072.x
Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis.
N. Pumplin (2010)
10.1007/s00299-010-0817-9
Two Arabidopsis cyclin A3s possess G1 cyclin-like features
I. Takahashi (2010)
10.1094/MPMI-06-10-0144
Conservation in function of a SCAR/WAVE component during infection thread and root hair growth in Medicago truncatula.
A. Miyahara (2010)
10.1104/pp.110.157800
Soybean Metabolites Regulated in Root Hairs in Response to the Symbiotic Bacterium Bradyrhizobium japonicum1[W][OA]
L. Brechenmacher (2010)
10.1073/pnas.0915001107
Bimodular auxin response controls organogenesis in Arabidopsis
I. De Smet (2010)
10.1105/tpc.110.075861
The Medicago truncatula E3 Ubiquitin Ligase PUB1 Interacts with the LYK3 Symbiotic Receptor and Negatively Regulates Infection and Nodulation[W][OA]
Malick Mbengue (2010)
10.1242/dev.051987
Strigolactones enhance competition between shoot branches by dampening auxin transport
S. Crawford (2010)
10.1038/ncomms1009
The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus
L. Madsen (2010)
10.1016/J.SOILBIO.2009.11.007
First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa)
M. Soto (2010)
The Medicago truncatula E 3 ubiquitin ligase PUB 1 interacts with the LYK 3 symbiotic receptor and negatively regulates infection and nodula - tion
M. Mbengue (2010)
10.1105/tpc.111.085464
Developmental Analysis of a Medicago truncatula smooth leaf margin1 Mutant Reveals Context-Dependent Effects on Compound Leaf Development[W][OA]
C. Zhou (2011)
10.1105/tpc.111.092049
GIGAS CELL1, a Novel Negative Regulator of the Anaphase-Promoting Complex/Cyclosome, Is Required for Proper Mitotic Progression and Cell Fate Determination in Arabidopsis[W]
E. Iwata (2011)
10.1105/tpc.111.089771
Strigolactone Biosynthesis in Medicago truncatula and Rice Requires the Symbiotic GRAS-Type Transcription Factors NSP1 and NSP2[W][OA]
Wei Liu (2011)
10.1111/j.1365-313X.2010.04415.x
Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula.
Jeremy D Murray (2011)
10.1073/pnas.1113992109
Legume pectate lyase required for root infection by rhizobia
F. Xie (2011)
10.1016/j.tplants.2010.12.001
Jasmonate-induced defenses: a tale of intelligence, collaborators and rascals.
C. Ballaré (2011)
10.1007/978-1-60761-682-5_13
Reverse genetics in medicago truncatula using Tnt1 insertion mutants.
X. Cheng (2011)
10.1126/science.1204903
Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity
Dongping Lu (2011)
10.1094/MPMI-12-10-0281
A dual-targeted soybean protein is involved in Bradyrhizobium japonicum infection of soybean root hair and cortical cells.
M. Libault (2011)
10.1146/annurev-genet-110410-132549
The rules of engagement in the legume-rhizobial symbiosis.
G. E. Oldroyd (2011)
10.1007/s00425-011-1516-7
Strigolactones promote nodulation in pea
E. Foo (2011)
10.1007/s00344-012-9304-6
Strigolactones: New Physiological Roles for an Ancient Signal
E. Foo (2012)
10.1104/pp.112.203190
Medicago truncatula ERN Transcription Factors: Regulatory Interplay with NSP1/NSP2 GRAS Factors and Expression Dynamics throughout Rhizobial Infection1[W]
Marion R Cerri (2012)
10.1038/nchembio.926
A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin
L. I. A. C. Villalobos (2012)
10.1104/pp.112.202572
Lotus japonicus ARPC1 Is Required for Rhizobial Infection1[W]
M. S. Hossain (2012)
10.1126/science.1213351
Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport
Li-Qing Chen (2012)
10.1111/j.1469-8137.2011.03989.x
Plant Aurora kinases play a role in maintenance of primary meristems and control of endoreduplication.
B. Petrovská (2012)
10.1111/j.1365-313X.2012.04946.x
The SAUR19 subfamily of SMALL AUXIN UP RNA genes promote cell expansion.
A. K. Spartz (2012)
10.1093/nar/gkr939
LegumeIP: an integrative database for comparative genomics and transcriptomics of model legumes
Jun Li (2012)
10.1104/pp.113.215111
Rhizobial Infection Is Associated with the Development of Peripheral Vasculature in Nodules of Medicago truncatula1[W][OA]
Dian Guan (2013)
10.1093/jxb/ert056
CAROTENOID CLEAVAGE DIOXYGENASE 7 modulates plant growth, reproduction, senescence, and determinate nodulation in the model legume Lotus japonicus
Junwei Liu (2013)
10.1371/journal.pgen.1003352
NODULE INCEPTION Directly Targets NF-Y Subunit Genes to Regulate Essential Processes of Root Nodule Development in Lotus japonicus
T. Soyano (2013)
10.1111/nph.12475
Host-specific Nod-factors associated with Medicago truncatula nodule infection differentially induce calcium influx and calcium spiking in root hairs
Giulia Morieri (2013)
10.1104/pp.113.220699
Ectopic Expression of miR160 Results in Auxin Hypersensitivity, Cytokinin Hyposensitivity, and Inhibition of Symbiotic Nodule Development in Soybean1[W][OPEN]
M. Turner (2013)
10.1111/1574-6968.12245
Invasion of rhizobial infection thread by non-rhizobia for colonization of Vigna radiata root nodules.
M. Pandya (2013)
10.1071/FP13123
Overexpression of miR160 affects root growth and nitrogen-fixing nodule number in Medicago truncatula.
Pilar Bustos-Sanmamed (2013)
10.1104/pp.113.223966
The Nodulation Factor Hydrolase of Medicago truncatula: Characterization of an Enzyme Specifically Cleaving Rhizobial Nodulation Signals1[W][OPEN]
Y. Tian (2013)
10.1093/jxb/ert392
The CCAAT box-binding transcription factor NF-YA1 controls rhizobial infection
P. Laporte (2014)
10.1105/tpc.113.120527
A H+-ATPase That Energizes Nutrient Uptake during Mycorrhizal Symbioses in Rice and Medicago truncatula[C][W][OPEN]
Ertao Wang (2014)
10.1105/tpc.113.120436
The H+-ATPase HA1 of Medicago truncatula Is Essential for Phosphate Transport and Plant Growth during Arbuscular Mycorrhizal Symbiosis[C][W][OPEN]
F. Krajinski (2014)
10.1111/nph.12575
An efficient reverse genetics platform in the model legume Medicago truncatula.
X. Cheng (2014)
10.3410/f.718415315.793504591
Faculty of 1000 evaluation for SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H -ATPases to Promote Cell Expansion in Arabidopsis.
S. Persson (2015)



This paper is referenced by
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K. Jarzyniak (2021)
10.3390/ijms22168495
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Debasis Mitra (2021)
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Yiteng Xu (2021)
10.1111/1751-7915.13906
Legume–rhizobium dance: an agricultural tool that could be improved?
L. Basile (2021)
10.1186/s12870-021-03060-z
An NADPH oxidase regulates carbon metabolism and the cell cycle during root nodule symbiosis in common bean (Phaseolus vulgaris)
Citlali Fonseca-García (2021)
10.3390/cells10020346
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Vinay Sharma (2021)
10.1007/s10265-021-01256-w
Involvement of Arachis hypogaea Jasmonate ZIM domain/TIFY proteins in root nodule symbiosis.
S. Sen (2021)
10.1101/2021.08.11.455944
A CCaMK/Cyclops response element in the promoter of L. japonicus Calcium-Binding Protein 1 (CBP1) mediates transcriptional activation in root symbioses
Xiaoyun Gong (2021)
10.1016/j.plantsci.2021.110846
The influence of ethylene, gibberellins and brassinosteroids on energy and nitrogen-fixation metabolites in nodule tissue.
Peter McGuiness (2021)
10.1016/j.pbi.2021.102026
Understanding Nod factor signalling paves the way for targeted engineering in legumes and non-legumes.
Christina Krönauer (2021)
10.3390/microorganisms9040774
Regulation of Plant Mineral Nutrition by Signal Molecules
V. Kalia (2021)
10.3390/genes12070988
The Effect of Exogenous Nitrate on LCO Signalling, Cytokinin Accumulation, and Nodule Initiation in Medicago truncatula
K. Gühl (2021)
10.3390/plants9010071
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Anil Kumar (2020)
10.1016/j.xplc.2020.100104
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Jie-shun Lin (2020)
10.3390/plants9030377
Biological and Cellular Functions of the Microdomain-Associated FWL/CNR Protein Family in Plants
S. Thibivilliers (2020)
10.1007/978-3-030-36248-5_1
The Rhizobium–Plant Symbiosis: State of the Art
Nitin Kumar (2020)
10.1093/jxb/eraa511
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Muhammad Zulfiqar Ahmad (2020)
10.1007/s00425-020-03478-z
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Peter McGuiness (2020)
10.1093/treephys/tpaa160
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Haibo Huo (2020)
10.15421/022014
The intensity of ethylene release by soybean plants under the influence of fungicides in the early stages of legume-rhizobial symbiosis
T. P. Mamenko (2020)
10.1186/s12870-020-02503-3
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Wenjuan Kang (2020)
10.3390/genes11070777
Evolution of NIN and NIN-like Genes in Relation to Nodule Symbiosis
J. Liu (2020)
10.3390/plants9020276
Molecular Basis of Root Nodule Symbiosis between Bradyrhizobium and ‘Crack-Entry’ Legume Groundnut (Arachis hypogaea L.)
Vinay Sharma (2020)
10.1016/j.xplc.2019.100019
A Roadmap toward Engineered Nitrogen-Fixing Nodule Symbiosis
R. Huisman (2020)
10.1111/nph.16950
Lotus japonicus Nuclear Factor YA1, a nodule emergence stage‐specific regulator of auxin signalling
Arina Shrestha (2020)
10.1093/femsec/fiaa222
Multi-species relationships in legume roots: From pairwise legume-symbiont interactions to the plant - microbiome - soil continuum.
M. Tsiknia (2020)
10.3389/fpls.2020.00592
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